From economy to luxury: Copper homeostasis in Chlamydomonas and other algae

Merchant, Sabeeha S.; Schmollinger, Stefan; Strenkert, Daniela; Moseley, Jeffrey L.; Blaby-Haas, Crysten E.

doi:10.1016/j.bbamcr.2020.118822

Title: From economy to luxury: Copper homeostasis in Chlamydomonas and other algae

Journal Article · Sun Nov 01 00:00:00 EDT 2020 · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research

DOI:https://doi.org/10.1016/j.bbamcr.2020.118822· OSTI ID:1828453

Merchant, Sabeeha S.; Schmollinger, Stefan; Strenkert, Daniela; Moseley, Jeffrey L.; Blaby-Haas, Crysten E.

Plastocyanin and cytochrome c6, abundant proteins in photosynthesis, are readouts for cellular copper status in Chlamydomonas and other algae. Their accumulation is controlled by a transcription factor copper response regulator (CRR1). The replacement of copper-containing plastocyanin with heme-containing cytochrome c6 spares copper and permits preferential copper (re)-allocation to cytochrome oxidase. Under copper-replete situations, the quota depends on abundance of various cuproproteins and is tightly regulated, except under zinc-deficiency where acidocalcisomes over-accumulate Cu(I). CRR1 has a transcriptional activation domain, a Zn-dependent DNA binding SBP-domain with a nuclear localization signal, and a C-terminal Cys-rich region that represses the zinc regulon. CRR1 activates >60 genes in Chlamydomonas through GTAC-containing CuREs; transcriptome differences are recapitulated in the proteome. The differentially-expressed genes encode assimilatory copper transporters of the CTR/SLC31 family including a novel soluble molecule, redox enzymes in the tetrapyrrole pathway that promote chlorophyll biosynthesis and photosystem 1 accumulation, and other oxygen-dependent enzymes, which may influence thylakoid membrane lipids, specifically polyunsaturated galactolipids and γ-tocopherol. Additionally, CRR1 also down-regulates 2 proteins in Chlamydomonas: for plastocyanin, by activation of proteolysis, while for the di-iron subunit of the cyclase in chlorophyll biosynthesis, through activation of an upstream promoter that generates a poorly-translated 5' extended transcript containing multiple short ORFs that inhibit translation. Furthermore, the functions of many CRR1-target genes are unknown, and the copper protein inventory in Chlamydomonas includes several whose functions are unexplored. The comprehensive picture of cuproproteins and copper homeostasis in this system is well-suited for reverse genetic analyses of these under-investigated components in copper biology.

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Research Organization:: Brookhaven National Laboratory (BNL), Upton, NY (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); National Institutes of Health (NIH)

Grant/Contract Number:: SC0012704; GM 042143

OSTI ID:: 1828453

Alternate ID(s):: OSTI ID: 1649988; OSTI ID: 1650680

Report Number(s):: BNL-216266-2020-JAAM; S0167488920301804; 118822; PII: S0167488920301804

Journal Information:: Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Journal Name: Biochimica et Biophysica Acta (BBA) - Molecular Cell Research Vol. 1867 Journal Issue: 11; ISSN 0167-4889

Publisher:: ElsevierCopyright Statement

Country of Publication:: Netherlands

Language:: English

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Systems Biology Approach in Chlamydomonas Reveals Connections between Copper Nutrition and Multiple Metabolic Steps Castruita, Madeli; Casero, David; Karpowicz, Steven J. The Plant Cell, Vol. 23, Issue 4 https://doi.org/10.1105/tpc.111.084400	journal	April 2011
Repression of ADH1 and ADH3 during zinc deficiency by Zap1-induced intergenic RNA transcripts Bird, Amanda J.; Gordon, Mat; Eide, David J. The EMBO Journal, Vol. 25, Issue 24 https://doi.org/10.1038/sj.emboj.7601453	journal	November 2006
Copper economy in Chlamydomonas : Prioritized allocation and reallocation of copper to respiration vs. photosynthesis Kropat, Janette; Gallaher, Sean D.; Urzica, Eugen I. Proceedings of the National Academy of Sciences, Vol. 112, Issue 9 https://doi.org/10.1073/pnas.1422492112	journal	February 2015
Microbial metalloproteomes are largely uncharacterized Cvetkovic, Aleksandar; Menon, Angeli Lal; Thorgersen, Michael P. Nature, Vol. 466, Issue 7307 https://doi.org/10.1038/nature09265	journal	July 2010
A regulator of nutritional copper signaling in Chlamydomonas is an SBP domain protein that recognizes the GTAC core of copper response element Kropat, J.; Tottey, S.; Birkenbihl, R. P. Proceedings of the National Academy of Sciences, Vol. 102, Issue 51 https://doi.org/10.1073/pnas.0507693102	journal	December 2005

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